How tardigrades come back from the dead

Tardigrades — aka water bears or moss piglets — are perhaps the most resilient creatures on the planet, able to survive complete dehydration, space vacuum and being frozen. However, only recently have scientists begun to unravel the genes that underpin the tardigrade's biological superpowers. “They’re 0.2mm to 1mm in length and despite being so small they are able to do all these things we cannot,” says Mark Blaxter, a biologist at the University of Edinburgh who has been studying tardigrades for 20 years. “In their DNA, they hold a cornucopia of secrets.”

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With Kazurahu Arakawa, from the University of Keio, Japan, Blaxter recently analysed the first true tardigrade genome. The results, published today in the open access journal PLOS Biology, are a first step towards explaining the genetics underpinning the tardigrade's extraordinary resilience and to pinpoint its place within the evolutionary tree of life. We spoke to Blaxter about his new research and his fascination for this remarkable little animal.

WIRED: How come we are only now able to analyse the tardigrade's true genomes?

MB: Two reasons. One is that, to most people, even fellow scientists, the genome of a tardigrade just isn’t that important. So tardigrades were not on the top of the list of things to be sequenced once the human genome was done. However, now that sequencing is so cheap and fast, those of us who are tardigrade enthusiasts can sequence them without needing millions of dollars to spend.

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How to catch a tardigrade

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The other reason we say we only have a “true” genome now (or a pair of true genomes) is because in 2015 a group at the University of North Carolina published what they claimed was the genome of the tardigrade Hypsibius dujardini. They also claimed that the genome was extraordinary because it contained lots of “foreign” genes, from bacteria and fungi and the like, that the tardigrade must have picked up along the evolutionary way. The process that moves these genes about is called horizontal gene transfer. The 2015 claim was that nearly one fifth of the tardigrade genes were foreign, a startling number. We have shown that this finding is wrong – their genome data was simply contaminated with bacteria and fungi and the like. Once the data is cleaned, all that is left is tardigrade with a very small number of genes that could be recently acquired by horizontal gene transfer from other organisms, which is a common finding. So we have debunked the “extensive” horizontal gene transfer story. But this does not mean that horizontal gene transfer does not happen. It is rare, but present, in many, many species.

Horizontal transfer is an exciting evolutionary mechanism, as it might allow an organism to acquire a whole new ability in one go, rather than have to slowly evolve it, small step by small step. Bacteria carry out horizontal transfer all the time. That is why multi-drug resistance and superbugs are such a threat: they swap the genes encoding antibiotic resistance. However, horizontal gene transfer between animals and bacteria is much rarer.

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Scanning electron microscope image of Ramazzottius varieornatus

Kazuharu Arakawa and Hiroki Higashiyama

An emerging theme is that genes that have been acquired by horizontal transfer from another species are often involved in some new aspect of biology. For example, both wood-eating beetles and plant-parasitic nematodes have acquired genes that enable them to digest cellulose - the core component of plant cell walls - from bacteria. It could be argued that these acquisitions are the eureka events that have allowed these species to take on a new lifestyle.

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The 2105 research paper was followed by suggestions that this heralded a whole new view of evolution, that the tree of life was more likely to be a net or web, with genes jumping all over the place. But there is no need for a new theory of evolution, the modern synthesis of Darwin’s natural selection and Mendel’s genetics still explains life on the planet.

What happens during desiccation at a molecular and genetic level, that allows tardigrades to survive?

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To live, or at least remain viable, without water, an organism has to ensure that the processes and structures that rely on water are somehow kept safe. In most organisms, if you dry them, the cell membranes collapse and proteins unfold and stick to each other, and there is no coming back from the dead if your membranes are gone and your proteins are clotted up.

The tardigrades

Hypsibius dujardini

A tardigrade usually found in freshwater ponds all over. The research team found theirs in a Manchester pond.

Ramazzottius varieornatus

A pink tardigrade found in algae and other crusts, again found all over. The research team's tardigrade was from Japan.

Tardigrades avoid the catastrophe of water loss by replacing water, which evaporates, with a substitute that cannot. In tardigrades, this substitute appears to be a set of proteins. Rather unusually, these proteins don’t have a defined structure. Most proteins fold in a very particular way in order to carry out their functions as enzymes or muscle proteins and so on. The “natively unstructured” proteins the tardigrades make appear to be a substitute for water – as the water is drawn out of the cells, the proteins probably wrap round enzymes to prevent them unfolding, coating the membranes to stop them collapsing in on themselves.

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What we found very interesting was that our two tardigrades use similar proteins but do things differently. Ramazzottius, a pink tardigrade, is able to withstand drying at zero notice. The pond tardigrade, Hypsibius dujardini, needs warning - if we dry it up rapidly it doesn’t survive, but if we give it 24-hours warning, by exposing it to a drying atmosphere, it does OK. Hypsibius has to turn on genes in order to survive drying, but Ramazzottius has already got the necessary proteins made.

Are tardigrades regularly subjected to dehydration in their normal environment? How?

Many tardigrades live in the sea, and in freshwater. These species don’t have the ability to dry out like the land tardigrades do. Tardigrades that live on land are really animals that live in a water film - the thin layer of water that coats soil particles, or covers the leaves of mosses. So maybe we can’t really call them “land animals”... they are definitely not “air animals”. The environments they live in are often frequently dried out - think of tardigrades on mosses on a wall, or tardigrades in the thin soil crust in a desert. When it rains, everything (moss, algae, tardigrades…) comes to life, eats, reproduces, etc, and then when the moss or soil dries out again, so do the tardigrades. It is going on every day all over the world – in your backyard, on the moss on the roof of your office building...

Does the discovery of these proteins have any potential applications in biotech and medicine?

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The proteins that allow the tardigrade cells to survive drying-out could be used to preserve cells and cell products “indefinitely” in a dried up state - no need for a freezer always on, or for the power never to short out.

For example, imagine a vaccine made in the UK that is to be used to protect kids from a devastating childhood disease across the developing world. Currently, we have to have a chain of fridges from here to, say, central Uganda – including a fridge in each and every village clinic, all of them working, every day – before we can be sure that the vaccine will get to the people who need it, safely and securely. Even then, the vaccine will have a shelf life, and we would have to guarantee it is kept cold all the time. Now imagine the same vaccine, coated in tardigrade desiccation proteins. Stored at room temperature and shipped by post, the vaccine would have a much-extended shelf life, and would be ready to use whenever and wherever it was needed.

What would happen if tardigrades were to disappear from the planet?

I would be very sad, as would generations of school children who use them for science projects, and amateur microscopists whose day is made when they see one.

More seriously, there are about a thousand species of tardigrade, most in the sea, and they likely perform roles in keeping soils and sediments ticking over. They can be locally very abundant in extreme environments like Antarctic mosses and desert crusts, and so they are especially important in some ecosystems. They eat bacteria, fungi and algae, and so act like the grazers on the plains of Africa – an essential link between the primary producers and the predators, keeping the system ticking over.

Because they can rehydrate and start their lives rapidly when it rains or unfreezes, it is likely they can be the first at the feast, and prosper while other species are just getting going.

You have been fascinated by these creatures for a while. Why?

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I have always loved small beasties, since I was a child. My parents bought me an Animal Encyclopaedia for Christmas and I especially pored over the weird and wonderful animals that were so beyond what I had (then) seen with my own eyes. I spent a lot of time looking at the obscure invertebrates in my Animal Encyclopaedia, and hoping to see them for real some day. This, it turns out, seems to have guided my research career.

I was reintroduced to tardigrades by a colleague, Aziz Aboobaker (now in Oxford), when we worked together in the 1990s. We had been working on how animals organised their bodies nose-to-tail, and he suggested we work on these tardigrades to try to work out how the odd patterns we were finding in roundworms had evolved. Once we had the tardigrades in the lab, we realised that these lovely animals could answer a lot of questions for us.